Skip to main content
SpringerLink
Log in

Phenotypic plasticity of abdomen pigmentation in two geographic populations of Drosophila melanogaster: male–female comparison and sexual dimorphism

  • Published:
Genetica Aims and scope Submit manuscript

Abstract

In Drosophila melanogaster male, the last abdominal tergites (A5–A6) are completely dark due to a strong internal constraint while, in female, all abdominal tergites (A2–A7) are phenotypically variable and highly plastic. Male A2–A4 are quite similar to those of female, but their plasticity was never investigated. In this paper, we compared the phenotypic plasticity of A2–A4 in both sexes in order to know if the major dimorphism (SD) expressed in male A5–A6 also extended toward the more anterior segments. We also compared two geographic populations living under very different climates in order to know if adaptive differences, previously observed in females also existed in males. With an isofemale line design, pigmentation variation according to growth temperature was investigated in the two populations from France and India. Male and female data were compared and sexual dimorphism (SD) analyzed in various ways. Reaction norms were quite similar in both sexes for A2 and A3, but clearly different for A4. Considering the total pigmentation (A2 + A3 + A4) males were darker than females at low temperatures and either identical to them (France) or lighter (India) above 25°C. SD (male–female difference) was genetically variable among lines and significantly different among segments. Reaction norms of SD exhibited an overall decrease with temperature and also a significant difference among populations, suggesting a local adaptation of SD to thermal conditions. The three plastic segments in male (A2–A4) seem to react adaptively to the thermal environment more efficiently than the same segments in female, in agreement with the thermal budget hypothesis. To our knowledge, it is the first time that a SD trait exhibits an adaptive difference between geographic populations.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Andrewartha HG, Birch LC (1954) The distribution and abundance of animals. University of Chicago Press, Chicago

    Google Scholar 

  • Bächli G (1971) Leucophenga und Paraleucophenga (Diptera Brachycera). Fondation pour favoriser les recherches scientifiques en Afrique, Bruxelles

    Google Scholar 

  • Baker BS, Ridge KA (1980) Sex and the single cell I On the action of major loci affecting cell determination in Drosophila melanogaster. Genetics 94:383–423

    PubMed  CAS  Google Scholar 

  • Capy P, David JR, Robertson A (1988) Thoracic trident pigmentation in natural populations of Drosophila simulans: a comparison with D. melanogaster. Heredity 61:263–268. doi:10.1038/hdy.1988.114

    Article  Google Scholar 

  • Capy P, Pla E, David JR (1994) Phenotypic and genetic variability of morphometrical traits in natural populations of Drosophila melanogaster and D. simulans. II. Within-population variability. Genet Sel Evol 26:15–28. doi:10.1051/gse:19940102

    Article  Google Scholar 

  • Cossins AR, Bowler K (1987) Temperature biology of animals. Chapman and Hall, London and New York

    Google Scholar 

  • David JR, Capy P (1988) Genetic variation of Drosophila melanogaster natural populations. Trends Genet 4:106–111

    CAS  Google Scholar 

  • David JR, Clavel MF (1965) Interaction entre le génotype et le milieu d’élevage. Conséquences sur les caractéristiques du développement de la Drosophile. Bull Biol Fr Belg 99:369–378

    Google Scholar 

  • David JR, Allemand R, Van Herrewege J, Cohet Y (1983) Ecophysiology: abiotic factors. In: Ashburner M, Carson HL, Thompson JN (eds) The genetics and biology of Drosophila. Academic Press, London, pp 105–170

    Google Scholar 

  • David JR, Capy P, Payant V, Tsakas S (1985) Thoracic trident pigmentation in Drosophila melanogaster: differentiation of geographical populations. Genet Sel Evol 17:211–223. doi:10.1051/gse:19850204

    Article  Google Scholar 

  • David JR, Capy P, Gauthier JP (1990) Abdominal pigmentation and growth temperatures in Drosophila melanogaster: similarities and differences in the norms of reaction of successive segments. J Evol Biol 3:429–445. doi:10.1046/j.1420-9101.1990.3050429.x

    Article  Google Scholar 

  • David JR, Moreteau B, Gauthier JR, Pétavy G, Stockel J, Imasheva A (1994) Reaction norms of size characters in relation to growth temperature in Drosophila melanogaster: an isofemale lines analysis. Genet Sel Evol 26:229–251. doi:10.1051/gse:19940305

    Article  Google Scholar 

  • David JR, Gibert P, Gravot E, Pétavy G, Morin JP, Karan D et al (1997) Phenotypic plasticity and developmental temperature in Drosophila: analysis and significance of reaction norms of morphometrical traits. J Therm Biol 22:441–451. doi:10.1016/S0306-4565(97)00063-6

    Article  Google Scholar 

  • David J, Gibert P, Mignon-Grasteau S, Legout H, Pétavy G, Beaumont C et al (2003) Genetic variability of sexual size dimorphism in a natural population of Drosophila melanogaster: an isofemale-line approach. J Genet 82:79–88. doi:10.1007/BF02715810

    Article  PubMed  Google Scholar 

  • David J, Gibert P, Legout H, Pétavy G, Capy P, Moreteau B (2005) Isofemale lines in Drosophila: an empirical approach to quantitative trait analysis in natural populations. Heredity 94:3–12. doi:10.1038/sj.hdy.6800562

    Article  PubMed  CAS  Google Scholar 

  • David JR, Legout H, Moreteau B (2006a) Phenotypic plasticity of body size in a temperate population of Drosophila melanogaster: when the temperature-size rule does not apply. J Genet 85:9–23. doi:10.1007/BF02728965

    Article  PubMed  Google Scholar 

  • David JR, Araripe LO, Bitner-Mathé BC, Capy P, Goni B, Klaczko LB et al (2006b) Sexual dimorphism of body size and sternopleural bristle number: a comparison of geographic populations of an invasive cosmopolitan drosophilid. Genetica 128:109–122. doi:10.1007/s10709-005-5539-5

    Article  PubMed  Google Scholar 

  • Falconer DS, Mackay TFC (1996) Introduction to quantitative genetics. Prentice Hall, England

    Google Scholar 

  • Gibert P, Moreteau B, Moreteau JC, David JR (1996) Growth temperature and adult pigmentation in two Drosophila sibling species: an adaptive convergence of reaction norms in sympatric populations? Evol Int J Org Evol 50:2346–2353. doi:10.2307/2410703

    Google Scholar 

  • Gibert P, Moreteau B, Moreteau JC, Parkash R, David JR (1998a) Light body pigmentation in Indian Drosophila melanogaster: a likely adaptation to a hot and arid climate. J Genet 77:13–20

    Article  Google Scholar 

  • Gibert P, Moreteau B, Scheiner SM, David JR (1998b) Phenotypic plasticity of body pigmentation in Drosophila: correlated variations between segments. Genet Sel Evol 30:181–194. doi:10.1051/gse:19980207

    Article  Google Scholar 

  • Gibert P, Moreteau B, Munjal AK, David JR (1999) Phenotypic plasticity of abdominal pigmentation in D kikkawai: multiple interaction between major gene, sex, abdomen segment and growth temperature. Genetica 105:165–176. doi:10.1023/A:1003704315194

    Article  PubMed  CAS  Google Scholar 

  • Gibert P, Moreteau B, David JR (2000) Developmental constraints on an adpative plasticity: reaction norms of pigmentation in adult segments of Drosophila melanogaster. Evol Dev 2:249–260. doi:10.1046/j.1525-142x.2000.00064.x

    Article  PubMed  CAS  Google Scholar 

  • Gibert P, Capy P, Imasheva A, Moreteau B, Morin J, Pétavy G et al (2004a) Comparative analysis of morphometrical traits among Drosophila melanogaster and D. simulans: genetic variability, clines and phenotypic plasticity. Genetica 120:165–179. doi:10.1023/B:GENE.0000017639.62427.8b

    Article  PubMed  CAS  Google Scholar 

  • Gibert P, Moreteau B, David JR (2004b) Phenotypic plasticity of body pigmentation in Drosophila melanogaster. Genetic repeatability of quantitative parameters in two successive generations. Heredity 92:499–507. doi:10.1038/sj.hdy.6800449

    Article  PubMed  CAS  Google Scholar 

  • Gibert JM, Personnet F, Schlötterer C (2007) Phenotypic plasticity in Drosophila pigmentation caused by temperature sensitivity of a chromatin regualr network. PLoS Genet 3:e30. doi:10.1371/journal.pgen.0030030

  • Gibson AR, Falls JB (1979) Thermal biology of the common garter snake Thamnophis sirtalis (L.). II. The effects of melanism. Oecologia 43:99–109. doi:10.1007/BF00346675

    Article  Google Scholar 

  • Hoffmann AA, Parsons PA (1988) The analysis of quantitative variation in natural populations with isofemale strains. Genet Sel Evol 20:87–98. doi:10.1051/gse:19880108

    Article  Google Scholar 

  • Hoffman AA, Parsons PA (1991) Evolutionary genetics and environmental stress. Oxford University Press, Oxford

    Google Scholar 

  • Hollocher H, Hatcher JL, Dyreson EG (2000) Evolution of abdominal pigmentation differences across species in the Drosophila dunni subgroup. Evol Int J Org Evol 54:2046–2056

    CAS  Google Scholar 

  • Huey RB, Moreteau B, Moreteau JC, Gibert P, Gilchrist GW, Ives AR et al (2006) Sexual size dimorphism in a Drosophila clade, the D. obscura group. Zoology 109:318–330. doi:10.1016/j.zool.2006.04.003

    Google Scholar 

  • Karan D, Morin JP, Gravot E, Moreteau B, David JR (1999) Body size reaction noms in Drosophila melanogaster temporal stability and genetic architecture in a natural population. Genet Sel Evol 31:491–508. doi:10.1051/gse:19990505

    Article  Google Scholar 

  • Kingsolver JG, Wiernasz DC (1991) Seasonal polyphenism in wing-melanin pattern and thermoregulatory adaptation in Pieris butterflies. Am Nat 137:816–830. doi:10.1086/285195

    Article  Google Scholar 

  • Klaczko LB (2006) Evolutionary genetics of Drosophila mediopunctata. Genetica 126:43–55. doi:10.1007/s10709-005-1431-6

    Article  PubMed  Google Scholar 

  • Kopp A, Duncan I, Godt D, Carroll S (2000) Genetic control and evolution of sexually dimorphic characters in Drosophila. Nature 408:553–559. doi:10.1038/35046017

    Article  PubMed  CAS  Google Scholar 

  • Kopp A, Graze R, Xu S, Carroll S, Nuzhdin S (2003) Quantitative trait loci responsible for variation in sexually dimorphic traits in Drosophila melanogaster. Genetics 163:771–787

    PubMed  CAS  Google Scholar 

  • Leather SR, Walters KFA, Bale JS (1993) The ecology of insect overwintering. Cambridge University Press, Cambridge

    Google Scholar 

  • Llopart A, Elwyn S, Lachaise D, Coyne J (2002) Genetics of a difference in pigmentation between Drosophila yakuba and Drosophila santomea. Evol Int J Org Evol 56:2262–2277

    CAS  Google Scholar 

  • Majerus MEN (1998) Melanism: evolution in action. Oxford Univ. Press, Oxford, UK

    Google Scholar 

  • Moreteau B, Gibert P, Pétavy G, Moreteau JC, Huey RB, David JR (2003) Morphometrical evolution in a Drosophila clade: the Drosophila obscura group. J Zool Syst Evol Res 41:64–71. doi:10.1046/j.1439-0469.2003.00195.x

    Article  Google Scholar 

  • Munjal AK, Karan D, Gibert P, Moreteau B, Parkash R, David JR (1997) Thoracic trident pigmentation in Drosophila melanogaster: latitudinal and altitudinal clines in Indian populations. Genet Sel Evol 29:601–610. doi:10.1051/gse:19970505

    Article  Google Scholar 

  • Precht H, Christophersen J, Hensel H, Larcher W (1973) Temperature and life. Springer Verlag, Berlin

    Google Scholar 

  • Reeve JP, Fairbairn DJ (1999) Change in sexual size dimorphism as a correlated response to selection on fecundity. Heredity 83:697–706. doi:10.1038/sj.hdy.6886160

    Article  PubMed  Google Scholar 

  • Roff DA (1992) The evolution of life histories theory and analysis. Chapman & Hall, London

    Google Scholar 

  • Rohmer C, David JR, Moreteau B, Joly D (2004) Heat induced male sterility in Drosophila melanogaster: adaptive genetic variations among geographic populations and role of the Y chromosome. J Exp Biol 207:2735–2743. doi:10.1242/jeb.01087

    Article  PubMed  Google Scholar 

  • True JR (2003) Insect melanism: the molecules matter. Trends Ecol Evol 18:640–647. doi:10.1016/j.tree.2003.09.006

    Article  Google Scholar 

  • Via S (1984) The quantitative genetics of polyphagy in an insect herbivore II. Genetic correlations in larval performance within and among host plants. Evol Int J Org Evol 38:896–905. doi:10.2307/2408399

    Google Scholar 

  • Watt WB (1969) Adaptive significance of pigment polymorphisms in Colias butterflies II. Thermoregulation and photoperiodically controlled melanin variation in Colias eurytheme. Proc Nat Acad Sci 63:767–774. doi:10.1073/pnas.63.3.767

    Article  Google Scholar 

  • Wittkop PJ, Carroll SB, Kopp A (2003) Evolution in black and white: genetic control of pigment patterns in Drosophila. Trends Genet 19:495–504. doi:10.1016/S0168-9525(03)00194-X

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Laboratoire de Biométrie et Biologie Evolutive, Université de Lyon, Université Lyon 1, CNRS, UMR 5558, 43 boulevard du 11 novembre 1918, Villeurbanne, 69622, France

    P. Gibert

  2. Laboratoire Evolution, Génome et Spéciation, CNRS, Avenue de la Terrasse, 91198, Gif sur Yvette Cedex, France

    B. Moreteau & J. R. David

  3. Université Paris-Sud 11, 91405, Orsay Cedex, France

    B. Moreteau & J. R. David

  4. Department Systematique et Evolution, Museum National d’Histoire Naturelle, UMR 5202 (OSEB), 45 rue Buffon, 75005, Paris, France

    J. R. David

Authors
  1. P. Gibert
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. B. Moreteau
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. J. R. David
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to P. Gibert.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Gibert, P., Moreteau, B. & David, J.R. Phenotypic plasticity of abdomen pigmentation in two geographic populations of Drosophila melanogaster: male–female comparison and sexual dimorphism. Genetica 135, 403–413 (2009). https://doi.org/10.1007/s10709-008-9286-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10709-008-9286-2

Keywords

Search

Navigation